Estuaries and Coasts

, Volume 42, Issue 1, pp 173–189 | Cite as

Assessment of Spatiotemporal Phytoplankton Composition in Relation to Environmental Conditions of Gorgan Bay, Iran

  • Zohreh Mazaheri Kouhanestani
  • Daniel L. RoelkeEmail author
  • Rasoul Ghorbani
  • Masami Fujiwara


Phytoplankton seasonal succession and spatial distribution were studied in Gorgan Bay, Iran, which is a semi-enclosed bay located in the southeastern Caspian Sea. Monthly phytoplankton and physicochemical samples were taken from March 2014 to September 2015. A total of 51 genera from six algal divisions were observed with phylum Bacillariophyta being the most represented (16 genera and on average ~ 59% of biomass). While diatoms were prevalent year-round, strong inter-seasonal variations of other phytoplankton groups were observed in response to environmental parameters. The seasonal succession of other taxa started with Chlorophyta (Chlorella sp.) in spring followed by Cyanophyta (Anabaena sp. and Microsystis sp.) and Euglenophyta (Euglena sp.) in summer, then Chrysophyta (Syndera) and Pyrrophyta (Prorocentrum sp., Exuviella sp., and Peridinium sp.) in the autumn and winter. The sites near the mouth of Gorgan Bay were characterized by slightly higher salinity with an annual mean of ~ 12 PSU compared with ~ 11 PSU for inner regions of the bay. Nitrate was higher in the mouth of the bay as well, with an annual mean of ~ 1.4 ppm compared with ~ 0.80 ppm in the inner region. Orthophosphate was also higher in the mouth of the bay with an annual mean of ~ 0.30 ppm compared with ~ 0.23 ppm in inner part of the bay. Euglena sp. and Microsystis sp. performed better in the mouth of the bay compared with their performance in the inner regions. Nutrients and salinity correlated strongest with phytoplankton in Gorgan Bay. During the period when Cyanophyta biomass was maximum, Microsystis sp. was the dominant taxa of the cyanobacteria present. Inorganic pollution from domestic wastewater in the eastern part of Gorgan Bay appears to be the cause of the Euglena maximum. According to the Palmer pollution index, Gorgan Bay experienced pollution from agricultural discharge and domestic wastewater.


Phytoplankton Seasonal variation Spatial heterogeneity Pollution Gorgan bay 



The authors thank Mr. Firouz Mehdipour for assistance in the field sampling. The authors also thank the Plankton Lab of Gorgan University of Agricultural Sciences and Natural Resource and Inland Waters Aquatic Stocks Research Center, which provided laboratory space and equipment for phytoplankton identification and nutrient analyses.


  1. Afshin, E. 1994. Iran rivers. Energy Ministry, Jamab, Tehran (in Persian).Google Scholar
  2. Ahn, C.Y., H.M. Oh, and Y.S. Park. 2011. Evaluation of environmental factors on cyanobacterial bloom in eutrophic reservoir using artificial neural networks. Journal of Phycology 47 (3): 495–504. Scholar
  3. Araghi, P.E., K.D. Bastami, and S. Rahmanpoor. 2014. Distribution and sources of polycyclic aromatic hydrocarbons in surface sediments of the Suez gulf. Marine Pollution Bulletin 89 (1–2): 494–498. Scholar
  4. Bagheri, S., M. Mansor, M. Makaremi, J. Sabkara, W.O.W. Maznah, A. Mirzajani, and S.H. Khodaparast. 2011. Fluctuations of phytoplankton community in the coastal waters of Caspian Sea in 2006. American Journal of Applied Sciences 8 (12): 1328–1336.Google Scholar
  5. Bagheri, S., M. Turkoglu, and A. Abedini. 2014. Seasonal changes of phytoplankton chlorophyl a, primary production and their relation in the continental shelf area of the south eastern Black Sea. Turkish. Journal of Fisheries and Aquatic Science 14: 713–726. Scholar
  6. Bashari, L., M. Gharaie, M. Hossein, R. Moussavi Harami, and H. Alizadeh Lahijani. 2014. Hydrogeochemical study of the Gorgan Bay and factors controlling the water chemistry. Oceanography 5: 31–42 (In Persian).Google Scholar
  7. Bastami, K.D., H. Bagheri, S. Haghparast, F. Soltani, A. Hamzehpoor, and M.D. Bastami. 2012. Geochemical and geo-statistical assessment of selected heavy metals in the surface sediments of the Gorgan Bay, Iran. Marine Pollution Bulletin 64 (12): 2877–2884. Scholar
  8. Bellinger, E., and D. Sigee. 2010. Algae as bioindicators. In Freshwater algae: Identification, enumeration and use as bioindicators, ed. E. Bellinger and D. Sigee. Hoboken: Wiley-Blackwell. 136pp.Google Scholar
  9. Belokda, W., K. Khalil, M. Loudiki, F. Aziz, and K. Elkalay. 2017. First assessment of phytoplankton diversity in a Morrocan shallow reservoir (Sidi Abderrahmane). Saudi Journal of Biological Sciences.
  10. Bharathi, M.D., V.V.S.S. Sarma, and K. Ramaneswari. 2018. Intra-annual variations in phytoplankton biomass and its composition in the tropical estuary: Influence of river discharge. Marine Pollution Bulletin 129 (1): 14–25. Scholar
  11. Boesch, D.F. 2002. Challenges and opportunities for science in reducing nutrient over-enrichment of coastal ecosystems. Estuaries 25 (4): 886–900. Scholar
  12. Brookes, J.D., and G.G. Ganf. 2001. Variations in the buoyancy response of Microcystis aeruginosa to nitrogen, phosphorus and light. Journal of Plankton Research 23 (12): 1399–1411. Scholar
  13. Bruesewitz, D.A., W.S. Gardner, R.F. Mooney, L. Pollard, and E.J. Buskey. 2013. Estuarine ecosystem function response to flood and drought in a shallow, semiarid estuary: Nitrogen cycling and ecosystem metabolism. Limnology and Oceanography 58 (6): 2293–2309. Scholar
  14. Chinnasamy, S., B. Ramakrishnan, A. Bhatnagar, and K.C. Das. 2009. Biomass production potential of a wastewater alga Chlorella vulgaris ARC 1 under elevated levels of CO2 and temperature. International Journal of Molecular Sciences 10 (2): 518–532. Scholar
  15. Chomérat, N., R. Garnier, C. Bertrand, and A. Cazaubon. 2007. Seasonal succession of cyanoprokaryotes in a hypereutrophic oligo-mesohaline lagoon from the south of France. Estuarine, Coastal and Shelf Science 72 (4): 591–602. Scholar
  16. Cloern, J.E., and A.D. Jassby. 2008. Complex seasonal patterns of primary producers at the land-sea interface. Ecology Letters 11 (12): 1294–1303. Scholar
  17. Cloern, J.E., and A.D. Jassby. 2010. Patterns and scales of phytoplankton variability in estuarine-coastal ecosystems. Estuaries and Coasts 33 (2): 230–241. Scholar
  18. Conley, D.J. 2000. Biogeochemical nutrient cycles and nutrient management strategies. Hydrobiologia 410: 87–96. Scholar
  19. Dorado, S., T. Booe, J. Steichen, A.S. McInnes, R. Windham, A. Shepard, A.E.B. Lucchese, H. Preischel, J.L. Pinckney, S.E. Davis, D.L. Roelke, and A. Quigg. 2015. Towards an understanding of the interactions between freshwater inflows and phytoplankton communities in a subtropical estuary in the Gulf of Mexico. PLoS One 10 (7): 1–23. Scholar
  20. Dvoretsky, V.G., and A.G. Dvoretsky. 2017. Macrozooplankton of the arctic—The Kara Sea in relation to environmental conditions. Estuarine, Coastal and Shelf Science 188: 38–55. Scholar
  21. Eaton, A.D., L.S. Clesceri, A.E. Greenberg, and M.A.H. Franson. 1998. Standard methods for the examination water and wastewater. Washington DC: American Public Health Association 1368p.Google Scholar
  22. Environmental Sciences Section (ESS). 1991. ESS Method 150.1. Chlorophyll-spectrophotometric. Inorganic Chemistry Unit. Wisconsin State Lab of Hygiene, Madison.
  23. Ganjian, A., W.O. Wan Maznah, K. Yahya, H. Fazli, M. Vahedi, A. Roohi, and S.M.V. Farabi. 2010. Seasonal and regional distribution of phytoplankton in the southern part of the Caspian Sea. Iranian Journal of Fisheries Sciences 9: 382–401.Google Scholar
  24. Gasinaite, Z.R., A.C. Cardoso, A.S. Heiskanen, P. Henriksen, P. Kauppila, I. Olenina, R. Pilkaityte, I. Purina, A. Razinkovas, S. Sagert, H. Schubert, and N. Wasmund. 2005. Seasonality of coastal phytoplankton in the Baltic Sea: Influence of salinity and eutrophication. Estuarine, Coastal and Shelf Science 65 (1-2): 239–252. Scholar
  25. Ghorbanzadeh Zaferani, S.G., A. Machinchian Moradi, R. Mousavi Nadushan, A.R. Sari, and S.M.R. Fatemi. 2016. Distribution pattern of heavy metals in the surficial sediment of Gorgan Bay (South Caspian Sea, Iran). Iranian Journal of Fisheries Sciences 15: 1144–1166.Google Scholar
  26. Ghorbanzadeh Zaferani, S.G., A. Machinchian Moradi, R. Mousavi Nadushan, A.R. Sari, and S.M.R. Fatemi. 2017. Spatial and temporal patterns of benthic macrofauna in Gorgan Bay, South Caspian Sea, Iran. Iran. J. Fish. Sci. 16: 274–252.Google Scholar
  27. Hillebrand, H., C.-D. Dürselen, D. Kirschtel, U. Pollingher, and T. Zohary. 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35 (2): 403–424. Scholar
  28. Hinder, S.L., G.C. Hays, M. Edwards, E.C. Roberts, A.W. Walne, and M.B. Gravenor. 2012. Changes in marine dinoflagellate and diatom abundance under climate change. Nature Climate Change 2 (4): 271–275. Scholar
  29. Ho, T.-Y., X. Pan, H.-H. Yang, G.T.F. Wong, and F.-K. Shiah. 2015. Controls on temporal and spatial variations of phytoplankton pigment distribution in the northern South China Sea. Deep Sea Research Part II: Topical Studies in Oceanography 117: 65–85. Scholar
  30. Hodgkiss, I.J., and S. Lu. 2004. The effects of nutrients and their ratios on phytoplankton abundance in Junk Bay, Hong Kong. Hydrobiologia 512: 215–229. Scholar
  31. Huang, L., W. Jian, X. Song, X. Huang, S. Liu, P. Qian, K. Yin, and M. Wu. 2004. Species diversity and distribution for phytoplankton of the Pearl River estuary during rainy and dry seasons. Marine Pollution Bulletin 49 (7-8): 588–596. Scholar
  32. Hubble, D.S., and D.M. Harper. 2002. Phytoplankton community structure and succession in the water column of Lake Naivasha, Kenya: a shallow tropical lake. Hydrobiologia 488 (1/3): 89–98. Scholar
  33. Huszar, V.L.M., and N.F. Caraco. 1998. The relationship between phytoplankton composition and physical–chemical variables: a comparison of taxonomic and morphological–functional descriptors in six temperate lakes. Freshwater Biology 40 (4): 679–696. Scholar
  34. Islam, M.S., J.S. Bonner, B.L. Edge, and C.A. Page. 2014. Hydrodynamic characterization of Corpus Christi Bay through modeling and observation. Environmental Monitoring and Assessment 186 (11): 7863–7876. Scholar
  35. Jamshidi, S., and N. Bin Abu Bakar. 2011. A study on distribution of chlorophyll-a in the coastal waters of Anzali Port, south Caspian Sea. Ocean Science Discussions 8: 435–451. Scholar
  36. Jamshidi, S. 2016. Study on physical and chemical characteristics of seawater of Gorgan Bay in the eastern part of southern coast of the Caspian Sea. In: Proceedings of academics world 44th international conference, Bangkok, Thailand, 13th–14th September 2016. pp. 17–21.Google Scholar
  37. Javani, A., H.T. Shahraeni, H. Mohammadkhani, B. Mansouri, and A.H. Tabari. 2014. Spatial and temporal fluctuation of nitrate and phosphate in Gorgan Bay. Environmental Science and Engineering 1: 1–13 (In Persian).Google Scholar
  38. Jindal, R., R.K. Thakur, U.B. Singh, A. Ahluwalia, R. Jindal, R. Thakur, U. Singh, and A. Ahluwalia. 2014a. Phytoplankton dynamics and water quality of Prashar Lake, Himachal Pradesh, India. Sustainability Water Quality and Ecology 3–4: 101–113. Scholar
  39. Jindal, R., R.K. Thakur, U.B. Singh, and A.S. Ahluwalia. 2014b. Phytoplankton dynamics and species diversity in a shallow eutrophic, natural mid-altitude lake in Himachal Pradesh (India): Role of physicochemical factors. Chemistry and Ecology 30 (4): 328–338. Scholar
  40. Kanoshina, I., U. Lips, and J.M. Leppänen. 2003. The influence of weather conditions (temperature and wind) on cyanobacterial bloom development in the Gulf of Finland (Baltic Sea). Harmful Algae 2 (1): 29–41. Scholar
  41. Karbassi, a.R., and R. Amirnezhad. 2004. Geochemistry of heavy metals and sedimentation rate in a bay adjacent to the Caspian Sea. International journal of Environmental Science and Technology 1 (3): 191–198. Scholar
  42. Kideys, A.E., N. Soydemir, E. Eker, V. Vladymyrov, D. Soloviev, and F. Melin. 2005. Phytoplankton distribution in the Caspian Sea during march 2001. Hydrobiologia 543 (1): 159–168. Scholar
  43. Kideys, A.E., A. Roohi, E. Eker-Develi, F. Mélin, and D. Beare. 2008. Increased chlorophyll levels in the southern Caspian Sea following an invasion of jellyfish. Research Letters in Ecology 2008: 1–4. Scholar
  44. Kurdi, M., T. Eslamkish, and M. Seyedali. 2015. Water quality evaluation and trend analysis in the Qareh Sou. Environment and Earth Science 73 (12): 8167–8175. Scholar
  45. Lahijani, H., O.H. Ardakani, A. Sharifi, and A.N. Bani. 2010. Sedimentological and geochemical characteristics of the Gorgan Bay sediments. Oceanography 1: 45–55 (in Persian).Google Scholar
  46. Liu, D. 2008. Phytoplankton diversity and ecology in estuaries of southeastern NSW, Australia. PhD thesis, University of Wollongong.Google Scholar
  47. Madhu, N.V., R. Jyothibabu, K.K. Balachandran, U.K. Honey, G.D. Martin, J.G. Vijay, C.A. Shiyas, G.V.M. Gupta, and C.T. Achuthankutty. 2007. Monsoonal impact on planktonic standing stock and abundance in a tropical estuary (Cochin backwaters – India). Estuarine, Coastal and Shelf Science 73: 54–64. Scholar
  48. Mahapatra, D.M., H.N. Chanakya, and T.V. Ramachandra. 2011. Assessment of treatment capabilities of Varthur Lake, Bangalore, India. International Journal of Environmental Technology and Management 14 (1/2/3/4): 84. Scholar
  49. Mahapatra, D.M., H.N. Chanakya, and T.V. Ramachandra. 2013. Euglena sp. as a suitable source of lipids for potential use as biofuel and sustainable wastewater treatment. Journal of Applied Phycology 25 (3): 855–865. Scholar
  50. Masoudi, M., R. Ramezannejad, and H. Riahi. 2012. Phytoplankton flora of Miankaleh wetland. Iran Journal of Botany 18: 141–148. Scholar
  51. Mehdipour, N., C. Wang, and M.H. Gerami. 2017. Spatio-temporal pattern of phytoplankton assemblages in the southern part of the Caspian Sea. Thalassas: An International Journal of Marine Sciences 33 (2): 99–108. Scholar
  52. Muylaert, K., K. Sabbe, and W. Vyverman. 2009. Changes in phytoplankton diversity and community composition along the salinity gradient of the Schelde estuary (Belgium/the Netherlands). Estuarine, Coastal and Shelf Science 82 (2): 335–340. Scholar
  53. NASA Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biology Processing Group. Moderate-resolution Imaging Spectroradiometer (MODIS) Aqua Photosynthetically Available Radiation Data. 2014. NASA OB.DAAC, Greenbelt, MD, USA., Accessed on 01/05/2018.
  54. Nasrollahzadeh, H.S., Z.B. Din, S.Y. Foong, and A. Makhlough. 2008a. Spatial and temporal distribution of macronutrients and phytoplankton before and after the invasion of the ctenophore, Mnemiopsis leidyi, in the Southern Caspian Sea. Chemistry and Ecology 24 (4): 233–246. Scholar
  55. Nasrollahzadeh, H.S., Z. Bin Din, S.Y. Foong, and A. Makhlough. 2008b. Trophic status of the Iranian Caspian Sea based on water quality parameters and phytoplankton diversity. Continental Shelf Research 28 (9): 1153–1165. Scholar
  56. Nasrollahzadeh, Hassan Saradi Makhlogh, A., Pourgholam, A., Vahedi, F., Qanqermeh, A., Foong, S.Y., 2011. The study of Nodularia Spumigena bloom event in the southern Caspian Sea. Applied Ecology and Environmental Research 9, 141–155.Google Scholar
  57. Nasrollahzadeh, H.S., A. Makhlough, F. Eslami, and A.G. Leroy Suzanne. 2014. Features of phytoplankton community in the southern Caspian Sea, a decade after the invasion of Mnemiopsis leidyi. Iranian Journal of Fisheries Sciences 13: 145–167.Google Scholar
  58. Nazeer, S., M.U. Khan, and R.N. Malik. 2018. Phytoplankton spatio-temporal dynamics and its relation to nutrients and water retention time in multi-trophic system of Soan River, Pakistan. Environmental Technology & Innovation 9: 38–50. Scholar
  59. O’Boyle, S., R. Wilkes, G. McDermott, S. Ní Longphuirt, and C. Murray. 2015. Factors affecting the accumulation of phytoplankton biomass in Irish estuaries and nearshore coastal waters: A conceptual model. Estuarine, Coastal and Shelf Science 155: 75–88. Scholar
  60. Oksanen, A.J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., Hara, R.B.O., Simpson, G.L., Solymos, P., Stevens, M.H.H., Wagner, H. 2015. Package vegan: Community ecology package [WWW Document]. ISBN 0-387-95457-0.Google Scholar
  61. Organization for Economic Cooperation and Development (OECD). 1982. Eutrophication of waters, monitoring, assessment and control. Paris: OECD Publications.Google Scholar
  62. Örnólfsdóttir, E.B., S.E. Lumsden, and J.L. Pinckney. 2004. Phytoplankton community growth-rate response to nutrient pulses in a shallow turbid estuary, Galveston Bay, Texas. Journal of Plankton Research 26: 325–339. Scholar
  63. Orr, P.T., G.J. Jones, and G.B. Douglas. 2004. Response of cultured Microcystis aeruginosa from the Swan River, Australia, to elevated salt concentration and consequences for bloom and toxin management in estuaries. Marine and Freshwater Research 55 (1/2/3/4): 277–283. Scholar
  64. Ozimek, T., R.D. Gulati, and E. van Donk. 1990. Can macrophytes be useful in biomanipulation of lakes? The Lake Zwemlust example. Hydrobiologia 200–201 (1): 399–407. Scholar
  65. Paerl, H.W. 1996. A comparison of cyanobacterial bloom dynamics in freshwater, estuarine and marine environments. Phycologia 35 (6S): 25–35. Scholar
  66. Paerl, H.W., and V.J. Paul. 2012. Climate change: Links to global expansion of harmful cyanobacteria. Water Research 46 (5): 1349–1363. Scholar
  67. Palmer, M. 1969. A composite rating of algae tolerating organic pollution. Journal of Phycology 5 (1): 78–82. Scholar
  68. Palmer, T.A., P.A. Montagna, J.B. Pollack, R.D. Kalke, and H.R. DeYoe. 2011. The role of freshwater inflow in lagoons, rivers, and bays. Hydrobiologia 667 (1): 49–67. Scholar
  69. Parab, S.G., P.S.G. Matondkar, M.F.H.D. Gomes, and Joaquim I. Goes. 2013. Effect of freshwater influx on phytoplankton in the Mandovi estuary (Goa, India) during monsoon season: Chemotaxonomy. Journal of Water Resource and Protection 5: 1076–1086. Scholar
  70. Pereira Coutinho, M.T., A.C. Brito, P. Pereira, A.S. Gonçalves, and M.T. Moita. 2012. A phytoplankton tool for water quality assessment in semi-enclosed coastal lagoons: Open vs closed regimes. Estuarine, Coastal and Shelf Science 110: 134–146. Scholar
  71. Preece, E.P., F.J. Hardy, B.C. Moore, and M. Bryan. 2017. A review of microcystin detections in estuarine and marine waters: Environmental implications and human health risk. Harmful Algae 61: 31–45. Scholar
  72. Quinlan, E.L., and E.J. Phlips. 2007. Phytoplankton assemblages across the marine to low salinity transition zone in a blackwater dominated estuary. Journal of Plankton Research 29: 401–416. Scholar
  73. R Development Core Team. 2017. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3900051-07-0.
  74. Rakocevic, J. 2012. Spatial and temporal distribution of phytoplankton in Lake Skadar. Archives of Biological Sciences 64 (2): 585–595. Scholar
  75. Ralston, D.K., and M.T. Stacey. 2005. Longitudinal dispersion and lateral circulation in the intertidal zone. Journal of Geophysical Research, C: Oceans 110: 1–17. Scholar
  76. Ranjbar, M.H., and N. Hadjizadeh Zaker. 2016. Estimation of environmental capacity of phosphorus in Gorgan Bay, Iran, via a 3D ecological-hydrodynamic model. Environmental Monitoring and Assessment 188 (11): 649. Scholar
  77. Ranjbar, M.H., and N. Hadjizadeh Zaker. 2018. Numerical modeling of general circulation, thermohaline structure, and residence time in Gorgan Bay, Iran. Ocean Dynamics 68 (1): 35–46. Scholar
  78. Reynold, C.S., and A.E. Walsby. 1975. Water blooms. Biological Reviews 50 (4): 437–481. Scholar
  79. Ringuet, S., and F.T. Mackenzie. 2005. Controls on nutrient and phytoplankton dynamics during normal flow and storm runoff conditions, southern Kaneo Bay, Hawaii. Estuaries 28 (3): 327–337. Scholar
  80. Roelke, D.L., H.-P. Li, N.J. Hayden, C.J. Miller, S.E. Davis, A. Quigg, and Y. Buyukates. 2013. Co-occurring and opposing freshwater inflow effects on phytoplankton biomass, productivity and community composition of Galveston Bay, USA. Marine Ecology Progress Series 477: 61–76.Google Scholar
  81. Roohi, A., A.E. Kideys, A. Sajjadi, A. Hashemian, R. Pourgholam, H. Fazli, A.G. Khanari, and E. Eker-Develi. 2010. Changes in biodiversity of phytoplankton, zooplankton, fishes and macrobenthos in the southern Caspian Sea after the invasion of the ctenophore Mnemiopsis Leidyi. Biological Invasions 12 (7): 2343–2361. Scholar
  82. Saghali, M., R. Baqraf, S.A. Hosseini, and R. Patimar. 2013. Benthic community structure in the Gorgan Bay (Southeast of the Caspian Sea, Iran): correlation to water physiochemical factors and heavy metal concentration of sediment. International Journal of Aquatic Biology 1: 245–253. Scholar
  83. Salem, Z., M. Ghobara, and A.A. El Nahrawy. 2017. Spatio-temporal evaluation of the surface water quality in the middle Nile Delta using Palmer’s algal pollution index. Egyptian Journal of Basic and Applied Sciences 4 (3): 219–226. Scholar
  84. Salmaso, N., Tolotti, M. 2009. Other phytoflagellates and groups of lesser importance. In Encyclopedia of inland waters, 174–183. Oxford: Academic Press.
  85. Shahryari, A., M.J. Kabir, and K.G. Firouzi. 2008. Evaluation of microbial pollution of Caspian Sea at the Gorgan Gulf. Journal of Gorgan University of Medical Sciences 10: 69–73.Google Scholar
  86. Sharbaty, S., 2012a. 3-D simulation flow pattern in the Gorgan Bay in during summer. International Journal of Engineering Research and Applications 2: 700–707.Google Scholar
  87. Sharbaty, S. 2012b. Two dimensional simulation of seasonal flow patterns in the Gorgan Bay. J. Basic Appl. Sci. Res. 2: 4382–4391.Google Scholar
  88. Shiganova, T.A., V.V. Sapozhnikov, E.I. Musaeva, and M.M. Domanov. 2003. Factors determining the conditions of distribution and quantitative characteristics of the ctenophore Mnemiopsis leidyi in the North Caspian Sea. Oceanology 43: 676–693.Google Scholar
  89. Singh, S.P., and P. Singh. 2015. Effect of temperature and light on the growth of algae species: A review. Renewable and Sustainable Energy Reviews 50: 431–444. Scholar
  90. Slate, J.E., and Stevenson, R.J. 2007. The diatom flora of phosphorus-enriched and unenriched sites in an Everglades Marsh. Biology Faculty Publications, Northeastern Illinois University, NEIU Digital Commons. 2. 56 pages.
  91. Smayda, T.J. 1997. Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnology and Oceanography 42 (5part2): 1137–1153. Scholar
  92. Sournia, A. 1978. Phytoplankton manual. Paris: UNESCO. 337p.Google Scholar
  93. Springer, J.J., J.M. Burkholder, P.M. Glibert, and R.E. Reed. 2005. Use of a real-time remote monitoring network (RTRM) and shipborne sampling to characterize a dinoflagellate bloom in the Neuse estuary, North Carolina, USA. Harmful Algae 4 (3): 533–551. Scholar
  94. Taheri, M., M.Y. Foshtomi, M. Noranian, and S.S. Mira. 2012. Spatial distribution and biodiversity of macrofauna in the southeast of the Caspian Sea, Gorgan Bay in relation to environmental conditions. Ocean Science Journal 47 (2): 113–122. Scholar
  95. Tango, P.J., R. Magnien, W. Butler, C. Luckett, M. Luckenbach, R. Lacouture, and C. Poukish. 2005. Impacts and potential effects due to Prorocentrum minimum blooms in Chesapeake Bay. Harmful Algae 4 (3): 525–531. Scholar
  96. Taukulis, F.E., and J. John. 2006. Diatoms as ecological indicators in lakes and streams of varying salinity from the wheatbelt region of Western Australia. Journal of the Royal Society of Western Australia 89: 17–25.Google Scholar
  97. Tonk, L., K. Bosch, P.M. Visser, and J. Huisman. 2007. Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquatic Microbial Ecology 46: 117–123. Scholar
  98. Utermöhl, H., 1936. Quantitativen methoden zur untersuchung des nanoplanktons. Abderhalden Handbuch der Biologischen Arbeitsmethoden 9: 1879–1937.Google Scholar
  99. Vadrucci, M.R., M. Cabrini, and A. Basset. 2007. Biovolume determination of phytoplankton guilds in transitional water ecosystems of mediterranean ecoregion. Transitional Waters Bulletin 1: 83–102. Scholar
  100. Vanni, M.J., and J. Temte. 1990. Seasonal patterns of grazing and nutrient limitation phytoplankton in a eutrophic lake. Limnology and Oceanography 35 (3): 697–709.Google Scholar
  101. Verspagen, J.M.H., J. Passarge, K.D. Jöhnk, P.M. Visser, L. Peperzak, P. Boers, H.J. Laanbroek, and J. Huisman. 2006. Water management strategies against toxic Microcystis blooms in the Dutch Delta. Ecological Applications 16 (1): 313–327. Scholar
  102. Vitousek, P.M., J.D. Aber, R.H. Howarth, G.E. Likens, P.A. Matson, D.W. Schindler, W.H. Schlesinger, and D.G. Tilman. 1997. Human alteration of the global nitrogen cycle: Source and consequences. Ecological Applications 7 (5): 737–750. Scholar
  103. Yin, K., P.Y. Qian, M.C.S. Wu, J.C. Chen, L. Huang, X. Song, and W. Jian. 2001. Shift from P to N limitation of phytoplankton growth across the Pearl River estuarine plume during summer. Marine Ecology Progress Series 221: 17–28. Scholar
  104. Zingone, A., E.J. Phlips, and P.J. Harrison. 2010. Multiscale variability of twenty-two coastal phytoplankton time series: A global scale comparison. Estuaries and Coasts 33 (2): 224–229. Scholar
  105. Zonn, I.S., A.N. Kosarev, M.H. Glantz, and Andrey G. Kostianoy. 2010. The Caspian Sea encyclopedia. 1st ed. Berlin: Springer. Scholar

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© Coastal and Estuarine Research Federation 2018

Authors and Affiliations

  1. 1.Department of Fisheries and Environmental SciencesGorgan University of Agricultural Sciences and Natural ResourcesGorganIran
  2. 2.Department of Wildlife and Fisheries SciencesTexas A&M UniversityCollege StationUSA
  3. 3.Department of OceanographyTexas A&M UniversityCollege StationUSA

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